Discussion
Although the trade-off between within-host infection load and
transmission is a central tenet of pathogen evolution (Alizon et al.,
2009), remarkably little is understood of this association in natural
populations, and under coinfection scenarios that are prevalent across
pathosystems (Tollenaere et al., 2016, Alizon et al., 2013). Here, we
study within-host disease load and between-host transmission
experimentally to understand how sensitive their association is to
pathogen strain identity and coinfection with a virus. We conduct a
survey of infection across 260 wild host populations to test whether our
experimental results are reflected in epidemiological patterns in the
wild.
Phomopsis subordinaria was detected in nearly half of the
surveyed natural host populations. The other fungal pathogen studied in
this same host population network - the powdery mildew fungus P.
plantaginis - infects annually 2-20% of P. lanceolatapopulations (Jousimo et al., 2014), and hence, by comparison P
subordinaria is relatively common. In few other wild plant
pathosystems, similar disease incidence rates have been observed (e.g.Triphragmium ulmariae rust infected 29-69% Filipendula
ulmaria host populations (Zhan et al., 2018), and Uromyces
valerianae rust infected 43-73% of Valeriana salina populations
(Ericson et al., 1999)). In our study, spatial structure was the main
determinant for pathogen incidence as both host population connectivity
and regional district explained variation in P. subordinariadistribution. Positive correlation between host connectivity and
infection incidence suggests that host population connectivity increases
between population transmission, as predicted by metapopulation theory
(Hanski, 1999). Large populations were more likely to be infected than
small populations, which is also in line with theoretical predictions
(Hanski, 1999). Unlike in P. plantaginis (Jousimo et al., 2014),
host population size did not have an effect on within-population
infection prevalence. While airborne pathogens such as P.
plantaginis are expected to be sensitive to host population size
through density-dependent transmission, P. subordinaria is
vector-transmitted and hence, is expected to be less responsive to
variation in host population size (Thrall et al., 1995). This result
highlights the importantance of the mode of transmission is for
epidemics.
Our field survey releveled extremely high within-host infection load
with 84% of host inflorescences being infected on average. While
within-host infection load was at its upper limits, transmission was
not, as the proportion of uninfected hosts was large. Majority of
epidemics were limited to less than 10% of hosts being within
populations. We did not find evidence of a trade-off between within-host
infection load and transmission limiting the spread of P.
subordinaria within its host populations. Instead, we found a positive
correlation between within-host disease load and population infection
prevalence. The observed low within-host populations prevalence ofP. subordinaria could also result from a range of other factors
unrelated to life-history correlations, including variation in host
plant susceptibility or pathogen infectivity (de Nooij & Damme, 1988),
constrained vector transmission (de Nooij, 1988, Pleydell et al., 2018),
and interactions with other pathogens than PlLV (Susi et al., 2015a,
Susi et al., 2015b).
Cross-kingdom coinfections are common (Lawn et al., 2006, Chen et al.,
2020) (Tollenaere et al., 2016, Tollenaere et al., 2017, Telfer et al.,
2010), and they are often suggested to have serious consequences in
disease epidemics and disease severity. The trade-offs observed under
single host–single pathogen scenarios may change under coinfection, as
host exploitation rates are expected to change under diverse infections
(Alizon et al., 2009). Plantago lanceolata is a host for a number
of pathogens in the Åland Islands, and coinfections are frequently
observed (Susi et al., 2015a, Susi et al., 2019). To understand how
coinfections may shape life-history correlations and disease dynamics ofP. subordinaria , we studied disease development under coinfection
with a recently characterized virus, PlLV. We found that coinfection
with virus had a profound impact on within-host infection load and
transmission of P. subordinaria that can further impact evolution
and epidemiology of the pathogen. Coinfection alleviated the harm caused
for the host and increased transmission potential. Under natural
epidemics such trade-offs could translate into low within-host disease
load and increased among host transmission.
The two strains differed significantly in their within-host infection
load, with strain P43 outperforming strain P29. Significant variation
among pathogens strains in their life-history traits is commonly
observed in natural pathogen populations (Tack et al., 2012). For both
strains, within-host infection load was lower under coinfection with
PlLV than when P. subordinaria infected the host alone, while
transmission potential was significantly higher under coinfection than
under single infection. The relationship between within-host infection
load and transmission potential was mediated by both strain identity and
coinfection. We observed a negative correlation between the measured
life-history stages in strain P29 suggesting a trade-off, whereas in
strain P43 there was no evidence of a trade-off. This result is in line
with previous research that found life-history correlations to be
depending on the pathogen genotype (Clement et al., 2012, Bruns et al.,
2014). The negative relationship between within-host infection load and
pycnidia formation became positive under coinfection. This is in line
with an earlier study testing coinfection with two strains of powdery
mildew fungus P. plantaginis where the strains had higher
performance and positive life-history trait correlations when challenged
with a competing strain (Laine & Mäkinen, 2018). Contrary to other
studies on coinfection where response to coinfection has been found
pathogen strain specific, here the response of the P.
subordinaria strains was similar. In bacteria –fluke coinfections on
salmons (Louhi et al., 2015), genotype specific responses on coinfection
were observed. Similarly, virus strain combinations resulted in
different within-host growth rates of bacterial pathogen on rice
(Tollenaere et al., 2017).
This study increases our understanding on the factors generating
diversity in epidemics in natural populations. Furthermore, this is one
of the very first reports addressing the knowledge gap on how pathogen
life-history traits correlate in realized epidemics. By showing that
pathogen coinfection and strain identity may alter life history
correlations this study contributes to better understanding of disease
evolution and epidemiology.